ReviewLactic acid bacteria – Potential for control of mould growth and mycotoxins: A review
Introduction
Mycotoxinogenic moulds such as Aspergillus, Fusarium and Penicillium play an undeniable role in the deterioration of the marketable quality and hygiene of foodstuffs by synthesizing highly toxic metabolites known as mycotoxins. Several of these toxins have been identified but quite a few could be responsible for significant problems in foodstuffs. Six classes of mycotoxins are frequently encountered in different food systems: aflatoxins, fumonisins, ochratoxins, patulin, trichothecenes and zearalenone. Concerning the importance and diversity of their toxic effects - carcinogenic, immunotoxic, teratogenic, neurotoxic, nephrotoxic and hepatotoxic - the occurrence of mycotoxinogenic moulds in foods is potentially dangerous for public health and also constitutes a major economic problem. For example, in Western Europe, the economic losses related to the presence of moulds in bread are estimated to be more than 200 million euros per year (Legan, 1993). Physical and chemical methods have been developed to control the occurrence of these microorganisms and their toxins, but no efficient strategy has yet been proposed to reduce the presence of mycotoxins. Moreover, some moulds have acquired the ability to resist chemical treatments and some preservatives. For example, some Penicillium can grow in the presence of potassium sorbate (Davidson, 2001) and other moulds possess the ability to degrade sorbate (Nielsen & de Boer, 2000). The reduction of such moulds in food production is thus of primary importance and there is great interest in developing efficient and safe strategies for this purpose. Biopreservation, the control of one organism by another, has received much attention in the last ten years (Magnusson, Ström, Roos, Sjögren, & Schnürer, 2003).
Among natural biological antagonists, LAB have several potential applications. These microorganisms are widely used for the production of fermented foods and are also part of intestinal microflora. Research reports indicate that LAB have beneficial health effects in humans. These bacteria have a long history of use in foods. They produce some antagonistic compounds able to control pathogenic bacteria and undesirable spoilage microflora, in particular. Using LAB to control mould growth could be an interesting alternative to physical and chemical methods because these bacteria have been reported to have strong antimicrobial properties. However, the antifungal activity of lactic strains remains to be elucidated. A limited number of reports have shown that a good selection of LAB could allow the control of mould growth and improve the shelf life of many fermented products and, therefore, reduce health risks due to exposure to mycotoxins (Gourama & Bullerman, 1995).
In this review, the ability of LAB to control mycotoxinogenic mould growth, the antifungal substances that have been characterised as of this time and the interactions of these organisms with some mycotoxins are successively investigated.
Section snippets
Lactic acid bacteria are able to control mycotoxinogenic mould growth
Due to their nutritional requirements, LAB are generally cultivated in enriched media and are found in dairy products, meat, meat-derived products and cereal products (Carr, Chill, & Maida, 2002). These bacteria are mainly divided into four genera: Lactococcus, Lactobacillus, Leuconostoc and Pediococcus. They are traditionally used as preservative agents to prevent spoilage and to extend the shelf life of food and feed.
According to Magnusson et al. (2003), three mechanisms may explain the
Factors that influence the antifungal activity of lactic acid bacteria
A well-designed selection of potential antifungal LAB could reduce the problem of toxinogenic moulds. However, relevant use of antifungal LAB requires thorough knowledge of the parameters that modulate their antifungal properties. Numerous parameters have been considered, including temperature, time of incubation, growth medium, pH and nutritional factors (Batish et al., 1997).
Antifungal metabolites produced by lactic acid bacteria
Several compounds with a strong antifungal activity have been isolated from bacterial cultures. As of this time, the majority of identified antifungal substances are low-molecular-weight compounds composed of organic acids, reuterin, hydrogen peroxide, proteinaceous compounds, hydroxyl fatty acids and phenolic compounds (Table 2).
Lactic acid bacteria–mycotoxin interactions
Most data dealing with the effects of LAB on the accumulation of mycotoxins are related to aflatoxin-producing moulds. Wiseman and Marth (1981) revealed the existence of an amensalism relationship between Lc. lactis and A. parasiticus. When these authors added the spores of A. parasiticus to a 13-day-old culture of Lc. lactis, they observed the entire repression of aflatoxin production. When the fungal spore suspension and the lactic strain were inoculated simultaneously, an increase in
Inhibition of mycotoxin biosynthesis by lactic acid bacteria
Several papers dealing with the inhibition of mycotoxin biosynthesis by LAB have focused on aflatoxins (Thyagaraja & Hosono, 1994). During cell lysis, it is possible that LAB releases molecules that potentially inhibit mould growth and therefore lead to a lower accumulation of their mycotoxins (Gourama & Bullerman, 1995). These “anti-mycotoxinogenic” metabolites could also be produced during LAB growth. Gourama (1991), using a dialysis assay, demonstrated the occurrence of a metabolite that
Binding of mycotoxins by lactic acid bacteria
The cell walls of some LAB such as Leuconostoc and Streptococcus have been reported to be able to bind some mutagenic compounds such as amino acid pyrolysates and heterocyclic amino acids produced during cooking. Similar results were obtained with other LAB isolated from fermented products (Rajendran and Ohta, 1998, Thyagaraja and Hosono, 1994). Further investigations have been conducted to evaluate the ability of LAB to remove other food-contaminating substances including mycotoxins, known for
Mechanism of mycotoxin binding by lactic acid bacteria
Few investigations have been conducted to elucidate the mechanism by which some mycotoxins such as aflatoxins, zearalenone and fumonisins are trapped by LAB pellets. It has been demonstrated that when heat or acid treatments were applied to LAB, their ability to remove aflatoxin B1 increased (El-Nezami et al., 1998). According to this result, supplementation of some basic compounds (NaOH and Na2CO3) and isopropanol was shown to negatively influence this binding. Viability of LAB strains was not
Stability of the lactic bacteria–mycotoxin complex
Potential future applications of LAB to reduce mycotoxin availability rely on the relative stability of the complexes formed. In the case of weak binding interactions, mycotoxins may be released by the continual washing of the bacterial surface in the gastrointestinal tract. Several studies have attempted to assess the stability of the complexes formed between mycotoxins and LAB and have concluded that the binding strength significantly depends on the strain and on environmental conditions.
Conclusion
The analysis of data available in the literature dealing with antifungal activity of LAB has highlighted the ability of some strains to repress mycotoxinogenic mould growth through the production of several low-molecular-weight antifungal metabolites. Even if some of these antifungal metabolites, including cyclic dipeptides, phenyllactic acids and 3-hydroxylated fatty acids, have been successfully purified, most of these low-molecular-mass compounds remain to be identified due to the lack of
Acknowledgements
This work is part of Doguiet Dalie’ PhD project financially supported by the “Ministère de l’Enseignement Supérieur et de la Recherche Scientifique” of Côte d’Ivoire, as part of the Integrated Research Project ‘‘Qualité Sanitaire des Aliments en Aquitaine 2006–2008”.
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